Covalent and Noncovalent Intermediates of an NAD Utilizing Enzyme, Human CD38

Chemistry and Biology

Volumn 15, Issue 10, 2008, Pages 1068-1078

  Liu, Qun ^a   Kriksunov, Irina A ^a   Jiang, Hong ^a   Graeff, Richard ^c   Lin, Hening ^a   Lee, Hon Cheung ^c,d   Hao, Quan ^a,b,d  

^a Department of Population Medicine and Diagnostic Sciences   (United States)

^b Department of Materials Science and Engineering   (United States)

^c UNIVERSITY OF MINNESOTA   (United States)

^d UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

CHEMBIO; PROTEINS

Indexed keywords

CD38 ANTIGEN; GLYCOSIDE; NICOTINAMIDE ADENINE DINUCLEOTIDE; NICOTINAMIDE NUCLEOTIDE;

ARTICLE; CATALYSIS; CHEMICAL STRUCTURE; CHEMISTRY; HUMAN; METABOLISM; PROTEIN BINDING; X RAY CRYSTALLOGRAPHY;

ANTIGENS, CD38; CATALYSIS; CRYSTALLOGRAPHY, X-RAY; GLYCOSIDES; HUMANS; MODELS, MOLECULAR; MOLECULAR STRUCTURE; NAD; NICOTINAMIDE MONONUCLEOTIDE; PROTEIN BINDING;

EID: 53849148622     PISSN: 10745521     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.chembiol.2008.08.007     Document Type: Article

References (49)

1. Aarhus R., Graeff R.M., Dickey D.M., Walseth T.F., and Lee H.C. ADP-ribosyl cyclase and CD38 catalyze the synthesis of a calcium-mobilizing metabolite from NADP. J. Biol. Chem. 270 (1995) 30327-30333
2. Berti P.J., Blanke S.R., and Schramm V.L. Transition state structure for the hydrolysis of NAD(+) catalyzed by diphtheria toxin. J. Am. Chem. Soc. 119 (1997) 12079-12088
3. Blander G., and Guarente L. The Sir2 family of protein deacetylases. Annu. Rev. Biochem. 73 (2004) 417-435
4. Bull H.G., Ferraz J.P., Cordes E.H., Ribbi A., and Apitzcastro R. Concerning Mechanism of Enzymatic and Non-Enzymatic Hydrolysis of Nicotinamide Nucleotide Coenzymes. J. Biol. Chem. 253 (1978) 5186-5192
5. Cakir-Kiefer C., Muller-Steffner H., and Schuber F. Unifying mechanism for Aplysia ADP-ribosyl cyclase and CD38/NAD(+) glycohydrolases. Biochem. J. 349 (2000) 203-210
6. Fukushi Y., Kato I., Takasawa S., Sasaki T., Ong B.H., Sato M., Ohsaga A., Sato K., Shirato K., Okamoto H., and Maruyama Y. Identification of cyclic ADP-ribose-dependent mechanisms in pancreatic muscarinic Ca(2+) signaling using CD38 knockout mice. J. Biol. Chem. 276 (2001) 649-655
7. Guse A.H. Second messenger function and the structure-activity relationship of cyclic adenosine diphosphoribose (cADPR). FEBS J. 272 (2005) 4590-4597
8. Handlon A.L., Xu C., Muller-Steffner H.M., Schuber F., and Oppenheimer N.J. 2′-Ribose Substituent Effects on the Chemical and Enzymatic-Hydrolysis of Nad(+). J. Am. Chem. Soc. 116 (1994) 12087-12088
9. Hassa P.O., Haenni S.S., Elser M., and Hottiger M.O. Nuclear ADP-ribosylation reactions in mammalian cells: where are we today and where are we going?. Microbiol. Mol. Biol. Rev. 70 (2006) 789-829
10. Howard M., Grimaldi J.C., Bazan J.F., Lund F.E., Santos-Argumedo L., Parkhouse R.M., Walseth T.F., and Lee H.C. Formation and hydrolysis of cyclic ADP-ribose catalyzed by lymphocyte antigen CD38. Science 262 (1993) 1056-1059
11. Jin D., Liu H.X., Hirai H., Torashima T., Nagai T., Lopatina O., Shnayder N.A., Yamada K., Noda M., Seike T., et al. CD38 is critical for social behaviour by regulating oxytocin secretion. Nature 446 (2007) 41-45
12. Jones T.A., Zou J.Y., Cowan S.W., and Kjeldgaard M. Improved methods for building protein models in electron-density maps and the location of errors in these models. Acta Crystallogr. A 47 (1991) 110-119
13. 2+]i, and insulin secretion. J. Biol. Chem. 274 (1999) 1869-1872
14. +. Mol. Cell. Biochem. 138 (1994) 229-235
15. Lee H.C. Enzymatic functions and structures of CD38 and homologs. Chem. Immunol. 75 (2000) 39-59
16. Lee H.C. Physiological functions of cyclic ADP-ribose and NAADP as calcium messengers. Annu. Rev. Pharmacol. Toxicol. 41 (2001) 317-345
17. 2+ stores: a perspective from cyclic ADP-ribose and NAADP. Curr. Mol. Med. 4 (2004) 227-237
18. Lee H.C. Structure and enzymatic functions of human CD38. Mol. Med. 12 (2006) 317-323
19. Lee H.C., Munshi C., and Graeff R. Structures and activities of cyclic ADP-ribose, NAADP and their metabolic enzymes. Mol. Cell. Biochem. 193 (1999) 89-98
20. 2+-mobilizing activity. J. Biol. Chem. 264 (1989) 1608-1615
21. Lee H.C., Zocchi E., Guida L., Franco L., Benatti U., and De Flora A. Production and hydrolysis of cyclic ADP-ribose at the outer surface of human erythrocytes. Biochem. Biophys. Res. Commun. 191 (1993) 639-645
22. Liu Q., Kriksunov I.A., Graeff R., Lee H.C., and Hao Q. Structural basis for formation and hydrolysis of the calcium messenger cyclic ADP-ribose by human CD38. J. Biol. Chem. 282 (2007) 5853-5861
23. Liu Q., Kriksunov I.A., Graeff R., Munshi C., Lee H.C., and Hao Q. Crystal structure of human CD38 extracellular domain. Structure 13 (2005) 1331-1339
24. Liu Q., Kriksunov I.A., Graeff R., Munshi C., Lee H.C., and Hao Q. Structural basis for the mechanistic understanding of human CD38-controlled multiple catalysis. J. Biol. Chem. 281 (2006) 32861-32869
25. Lombard D.B., Chua K.F., Mostoslavsky R., Franco S., Gostissa M., and Alt F.W. DNA repair, genome stability, and aging. Cell 120 (2005) 497-512
26. Michan S., and Sinclair D. Sirtuins in mammals: insights into their biological function. Biochem. J. 404 (2007) 1-13
27. Mitsui-Saito M., Kato I., Takasawa S., Okamoto H., and Yanagisawa T. CD38 gene disruption inhibits the contraction induced by alpha-adrenoceptor stimulation in mouse aorta. J. Vet. Med. Sci. 65 (2003) 1325-1330
28. Muller-Steffner H.M., Augustin A., and Schuber F. Mechanism of cyclization of pyridine nucleotides by bovine spleen NAD(+) glycohydrolase. J. Biol. Chem. 271 (1996) 23967-23972
29. Munshi C., Aarhus R., Graeff R., Walseth T.F., Levitt D., and Lee H.C. Identification of the enzymatic active site of CD38 by site-directed mutagenesis. J. Biol. Chem. 275 (2000) 21566-21571
30. Murshudov G.N., Vagin A.A., and Dodson E.J. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D Biol. Crystallogr. 53 (1997) 240-255
31. O'Neal C.J., Jobling M.G., Holmes R.K., and Hol W.G. Structural basis for the activation of cholera toxin by human ARF6-GTP. Science 309 (2005) 1093-1096
32. Oppenheimer N.J. NAD hydrolysis: chemical and enzymatic mechanisms. Mol. Cell. Biochem. 138 (1994) 245-251
33. Otwinowski Z., and Minor W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276 (1997) 307-326
34. Partida-Sanchez S., Cockayne D.A., Monard S., Jacobson E.L., Oppenheimer N., Garvy B., Kusser K., Goodrich S., Howard M., Harmsen A., et al. Cyclic ADP-ribose production by CD38 regulates intracellular calcium release, extracellular calcium influx and chemotaxis in neutrophils and is required for bacterial clearance in vivo. Nat. Med. 7 (2001) 1209-1216
35. Partida-Sanchez S., Goodrich S., Kusser K., Oppenheimer N., Randall T.D., and Lund F.E. Regulation of dendritic cell trafficking by the ADP-ribosyl cyclase CD38: impact on the development of humoral immunity. Immunity 20 (2004) 279-291
36. Rai K.R., Peterson B.L., Appelbaum F.R., Kolitz J., Elias L., Shepherd L., Hines J., Threatte G.A., Larson R.A., Cheson B.D., and Schiffer C.A. Fludarabine compared with chlorambucil as primary therapy for chronic lymphocytic leukemia. N. Engl. J. Med. 343 (2000) 1750-1757
37. Sauve A.A., Deng H.T., Angeletti R.H., and Schramm V.L. A covalent intermediate in CD38 is responsible for ADP-ribosylation and cyclization reactions. J. Am. Chem. Soc. 122 (2000) 7855-7859
38. Sauve A.A., Munshi C., Lee H.C., and Schramm V.L. The reaction mechanism for CD38. A single intermediate is responsible for cyclization, hydrolysis, and base-exchange chemistries. Biochemistry 37 (1998) 13239-13249
39. Sauve A.A., and Schramm V.L. Mechanism-based inhibitors of CD38: a mammalian cyclic ADP-ribose synthetase. Biochemistry 41 (2002) 8455-8463
40. Sauve A.A., and Schramm V.L. SIR2: the biochemical mechanism of NAD(+)-dependent protein deacetylation and ADP-ribosyl enzyme intermediates. Curr. Med. Chem. 11 (2004) 807-826
41. Schuber F., and Lund F.E. Structure and enzymology of ADP-ribosyl cyclases: conserved enzymes that produce multiple calcium mobilizing metabolites. Curr. Mol. Med. 4 (2004) 249-261
42. Schuttelkopf A.W., and van Aalten D.M. PRODRG: a tool for high-throughput crystallography of protein-ligand complexes. Acta Crystallogr. D Biol. Crystallogr. 60 (2004) 1355-1363
43. Seman M., Adriouch S., Haag F., and Koch-Nolte F. Ecto-ADP-ribosyltransferases (ARTs): emerging actors in cell communication and signaling. Curr. Med. Chem. 11 (2004) 857-872
44. + analogs containing a 2′-deoxy-2′-substituted nicotinamide arabinofuranosyl moiety. J. Org. Chem. 56 (1991) 3608-3613
45. Smith B.C., and Denu J.M. Sir2 protein deacetylases: evidence for chemical intermediates and functions of a conserved histidine. Biochemistry 45 (2006) 272-282
46. Sun L., Iqbal J., Dolgilevich S., Yuen T., Wu X.B., Moonga B.S., Adebanjo O.A., Bevis P.J., Lund F., Huang C.L., et al. Disordered osteoclast formation and function in a CD38 (ADP-ribosyl cyclase)-deficient mouse establishes an essential role for CD38 in bone resorption. FASEB J. 17 (2003) 369-375
47. + glycohydrolase-catalyzed reactions. Bioorg. Chem. 16 (1988) 38-51
48. +-glycohydrolase-catalyzed hydrolysis of pyridine dinucleotides. Bioorg. Chem. 15 (1987) 31-42
49. Versees W., Loverix S., Vandemeulebroucke A., Geerlings P., and Steyaert J. Leaving group activation by aromatic stacking: an alternative to general acid catalysis. J. Mol. Biol. 338 (2004) 1-6